Species interactions drive diverse evolutionary outcomes. Speciation by cascade reinforcement represents one example of how species interactions can contribute to the proliferation of species. This process occurs when the divergence of mating traits in response to selection against interspecific hybridization incidentally leads to reproductive isolation among populations of the same species. Here, we investigated the population genetic outcomes of cascade reinforcement in North American chorus frogs (Hylidae:
- Award ID(s):
- 1655935
- NSF-PAR ID:
- 10095552
- Date Published:
- Journal Name:
- Ecology and evolution
- Volume:
- 8
- ISSN:
- 2045-7758
- Page Range / eLocation ID:
- 2852–2867
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Pseudacris ). Specifically, we estimated the frequency of hybridization among three taxa, assessed genetic structure within the focal species,P .feriarum , and ascertained the directionality of gene flow withinP .feriarum across replicated contact zones via coalescent modeling. Through field observations and preliminary experimental crosses, we assessed whether hybridization is possible under natural and laboratory conditions. We found that hybridization occurs amongP .feriarum and two conspecifics at a low rate in multiple contact zones, and that gene flow within the former species is unidirectional from allopatry into sympatry with these other species in three of four contact zones studied. We found evidence of substantial genetic structuring withinP .feriarum including a divergent western allopatric cluster, a behaviorally‐distinct sympatric South Carolina cluster, and several genetically‐overlapping clusters from the remainder of the distribution. Furthermore, we found sub‐structuring between reinforced and nonreinforced populations in the two most intensely‐sampled contact zones. Our literature review indicated thatP .feriarum hybridizes with at least five heterospecifics at the periphery of its range providing a mechanism for further intraspecific diversification. This work strengthens the evidence for cascade reinforcement in this clade, revealing the geographic and genetic landscape upon which this process can contribute to the proliferation of species. -
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Abstract When two species are incompletely isolated, strengthening premating isolation barriers in response to the production of low fitness hybrids may complete the speciation process. Here, we use the sister species
Drosophila subquinaria andDrosophila recens to study the conditions under which this reinforcement of species boundaries occurs in natural populations. We first extend the region of known sympatry between these species, and then we conduct a fine‐scale geographic survey of mate discrimination coupled with estimates of gene flow within and admixture between species. WithinD. subquinaria , reinforcement is extremely effective: we find variation in mate discrimination both againstD. recens males and against conspecific allopatric males on the scale of a few kilometres and in the face of gene flow both from conspecific populations and introgression fromD. recens . InD. recens , we do not find evidence for increased mate discrimination in sympatry, even whereD. recens is rare, consistent with substantial gene flow throughout the species’ range. Finally, we find that introgression between species is asymmetric, with more fromD. recens intoD. subquinaria than vice versa. Within each species, admixture is highest in the geographic region where it is rare relative to the other species, suggesting that when hybrids are produced they are of low fitness. In sum, reinforcement withinD. subquinaria is effective at maintaining species boundaries, but even when reinforcing selection is strong it may not always result in a pattern of strong reproductive character displacement due to variation in the frequency of hybridization and gene flow from neighbouring populations. -
Reproductive isolation is necessary for population divergence to lead to the formation of separate species. This can occur due to physical isolation of populations, which drives allopatric speciation, or other methods of isolation, such as sympatric speciation where the diverging species are physically in the same range, but structural genomic changes or mutations cause the population to diverge into two different species. Parapatric speciation occurs when populations that are geographically adjacent to each other diverge, which can be driven by adaptations to environmental differences, even with ongoing gene flow. Two desert- adapted brittlebush species, Encelia farinosa and Encelia californica, diverged less than 1 million years ago (Singhal et al., 2020) and have a parapatric distribution, residing in different environments in the Mojave and Sonoran deserts. Encelia farinosa (Brittlebush) has unique silvery leaves that are covered in tiny hairs (leaf pubescence) to better control leaf temperature in the hot and arid conditions of the Sonoran Desert. Encelia californica (California Brittlebush) does not display leaf pubescence and is found in a smaller region of the Mediterranean-like environment of the west coast of North America. Encelia californica is exposed to more precipitation than most other Encelia species. Even with their different morphologies, these two species are still able to hybridize and create fertile offspring (Clark, 1998). Using PacBio sequencing and Hi-C scaffolding, we assembled and annotated reference genomes for both species to investigate the genomic basis of reproductive isolation in these two species. The scaffold N50/L50 are 10 scaffolds and 76.3 Mbp, and 12 scaffolds and 64.5 Mbp for E. farinosa and E. californica, respectively. Using comparative genomic analyses such as tests for differential adaptation and chromosomal translocations will help reveal whether the drivers of speciation in the Encelia radiation were external (e.g., geologic/climatic) or internal (e.g., genomic rearrangement). These analyses will also help answer how accumulated genomic differences can cause speciation in populations that are not geographically isolated. Analyses such as these are new, exciting sources of information for testing geogenomic and other Earth- life hypotheses.more » « less
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Abstract The role of sexual selection in speciation is implicated in both empirical case studies and larger comparative works. However, sexual selection faces two major problems in driving speciation. First, because females with novel preferences search for their initially rare males, search costs are expected to curtail initial sexual divergence. Second, if these populations come back into sympatry, sexual divergence may be erased due to hybridization. A major goal is to understand which conditions increase the likelihood of overcoming these problems. Here we generated a diploid population genetic model of how female search costs and evolution of female ‘choosiness’ (i.e. preference strength) interact to drive speciation in allopatry and secondary contact. We studied the model using numerical simulations in the context of two different male traits, ecologically ‘arbitrary’ versus ‘magic’ traits. First, in allopatry, without female search costs only minor and fluctuating sexual isolation evolved. In contrast, with female search costs, sexual isolation was highly curtailed with arbitrary male traits but was greatly facilitated with magic traits. However, because search costs selected for reduced choosiness, sexual isolation with magic traits was eventually eroded, the rate determined by the genetic architecture of choosiness. These factors also played a key role in secondary contact; with evolvable choosiness and female search costs, pure sexual selection models collapsed upon secondary contact. However, when we added selection against hybrids (i.e. reinforcement) to this model, we found that speciation could be maintained under a wide range of conditions with arbitrary male traits, but not with magic male traits. This surprisingly suggests that arbitrary male traits are in some cases more likely to aid speciation than magic male traits. We discuss these findings and relate them to empirical literature on female choosiness within species and in hybrids.
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• Reinforcement is the process through which prezygotic reproductive barriers evolve in sympatry due to selection against hybridization between co-occurring, closely related species. The role of self-fertilization in reinforcement and reproductive isolation is uncertain in part because its efficiency as a barrier against heterospecific mating can depend on the timing of autonomous selfing. • To investigate whether increased autonomous selfing has evolved as a mechanism for reinforcement, we compared Phlox cuspidata populations across their native Texas range using both estimates of genetic diversity and experimental manipulation with morphological measurements. Specifically, we investigated patterns of variation in floral traits and timing of selfing between individuals from allopatric populations of P. cuspidata and from populations sympatric with the closely related species, P. drummondii. • We infer intermediate rates of selfing across field-collected individuals with no significant difference between allopatric and sympatric populations. Among greenhouse grown plants, we find no differences in timing of selfing or other floral traits including anther dehiscence timing, anther-stigma distances, autonomous selfing rate and self-seed count between allopatric and sympatric populations. However, our statistical analyses indicate that P. cuspidata individuals sympatric with P drummondii seem to have generally larger flowers compared to allopatric individuals. • Despite strong evidence of costly hybridization with P. drummondii, we find no evidence of trait divergence due to reinforcement in P. cuspidata. Although we document nearly complete autonomous self-seed set in the greenhouse, estimates of selfing rates from genetic data imply realized selfing is much lower in nature suggesting an opportunity for reinforcing selection to act on this trait.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/DOI: 10.1002/ece3.3893
